JAC-

Antimicrobial
Resistance
JAC Antimicrob Resist
doi:10.1093/jacamr/dlab003

Antimicrobial resistance among uropathogens in the Asia-Pacific

region: a systematic review
1
Adhi Kristianto Sugianli *, Franciscus Ginting2, Ida Parwati1, Menno D. de Jong3, Frank van Leth4,5 and
Constance Schultsz3,4,5

1
Department of Clinical Pathology, Faculty of Medicine, Universitas Padjadjaran, Hasan Sadikin General Hospital, Bandung, Indonesia;

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

2
Department of Internal Medicine, Faculty of Medicine, Universitas Sumatera Utara, Adam Malik General Hospital, Medan, Indonesia;
3
Department of Medical Microbiology, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands;
4
Department of Global Health, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands;
5
Amsterdam Institute for Global Health and Development, Amsterdam, The Netherlands

*Corresponding author. E-mail: adhi.kristianto@unpad.ac.id

Received 21 July 2020; accepted 4 January 2021

Background: Antimicrobial resistance (AMR) in urinary tract infections (UTI) is a global public health problem.
However, estimates of the prevalence of AMR, required for empirical treatment guidelines, are lacking for many
regions.
Objectives: To perform a systematic review and summarize the available information about AMR prevalence
among urinary Escherichia coli and Klebsiella pneumoniae, the two priority uropathogens, in the Asia-Pacific
region (APAC).
Methods: PubMed, EBSCO and Web of Science databases were searched for articles (2008–20), following
PRISMA guidelines. The prevalence of resistance was calculated and reported as point estimate with 95% CI for
antimicrobial drugs recommended in WHO treatment guidelines. Data were stratified by country and surveil-
lance approach (laboratory- or population-based surveillance). The quality of included articles was assessed
using a modified Newcastle-Ottawa Quality Assessment Scale.
Results: Out of 2400 identified articles, 24 studies, reporting on 11 (26.8%) of the 41 APAC countries, met the in-
clusion criteria. Prevalence of resistance against trimethoprim/sulfamethoxazole, ciprofloxacin, and ceftriaxone
ranged between 33% and 90%, with highest prevalence reported from Bangladesh, India, Sri Lanka and
Indonesia. Resistance against nitrofurantoin ranged between 2.7% and 31.4%. Two studies reported data on
fosfomycin resistance (1.8% and 1.7%). Quality of reporting was moderate.
Conclusions: We show very high prevalence estimates of AMR against antibiotics commonly used for the empir-
ical treatment of UTI, in the limited number of countries in the APAC for which data are available. Novel feasible
and affordable approaches that facilitate population-based AMR surveillance are needed to increase knowledge
on AMR prevalence across the region.

Introduction
Antimicrobial resistance (AMR) is a global public health
threat.1,2 Most of the direct and indirect burden of AMR is antici-
pated in low- and middle-income countries due to several fac-
tors, including lack of surveillance capacity and systematic data
collection of AMR.3,4 The Asia-Pacific region (APAC), which
comprises the South-East Asia and Western Pacific Regions, is
considered at high risk and a hotspot for the spread of AMR.4
The AMR in APAC affects both the low-to-middle-income
countries and high-income countries in this region.
Urinary tract infections (UTIs) are common bacterial infec-
tions that occur both in the community and in hospitals. UTIs
are mostly treated empirically and lead the rising prevalence
of AMR.5,6 The effectiveness of empirical treatment is depend-
ent on the underlying prevalence of resistance in the most
common causative pathogens, which is often unknown due to

C The Author(s) 2021. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy.
V
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/
by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
1 of 12
Systematic review
lack of diagnostics, or is based on laboratory-based surveillance
data only.5,6 We have previously shown in a population-based
surveillance in Indonesia that the prevalence of AMR in the main
urinary pathogens Escherichia coli and Klebsiella pneumoniae is
extremely high (more than 50%) in both in-patients and out-
patients, with a prevalence of resistance ,20% only for tigecycline
and fosfomycin.7 These results raise concerns about the prevalence
of AMR in urinary pathogens in other countries in the region.
Given the current unavailability of published national surveil-
lance data for most countries, the aim of this systematic
review is to summarize the available information about AMR
prevalence among E. coli and K. pneumoniae isolated from
patients suspected of UTI in the APAC, to inform clinical practice
with regard to empirical treatment and to identify the main
knowledge gaps. We focused our review on the combination
of E. coli and K. pneumoniae given the fact that these two
pathogens together cause up to 80% of UTIs, and as per WHO
recommendations.1
Figure 1. Flow chart of the systematic review process (PRISMA).
2 of 12
Methods
Search strategy
We searched PubMed, EBSCO, and Web of Science in the time period
between 1 January 8 and 5 January 2020. The search strategy included the
combination of the following keywords with free text search category: ‘anti-
microbial resistance’, ‘surveillance’, ‘survey’, ‘prevalence’, ‘epidemiology’
and ‘UTI’. The detailed search strategy is provided in Method 1 (available as
Supplementary data at JAC-AMR Online). Our search strategy did not in-
clude limits for countries of the Asia-Pacific region but instead, this selection
was made as part of the inclusion process.
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
Selection criteria
Articles were screened by title and abstract to select those for full text as-
sessment. Studies were included for analysis if they fulfilled the following
criteria:
1. Describe AMR in bacterial isolates from human patients with symp-
tomatic UTI (upper or lower).
Systematic review JAR
Table 1. Quality assessment of included articles

Definition Representativeness
of population of the sample Ascertainment of AST method

Are the criteria Is the sampling Does the

Is the study (case definition) of the study study describe Did the study Did the study
population for enrolment population the method for specify the report on internal
clearly in the study clearly susceptibility breakpoint quality control
Author Reference Year described? clearly stated? described? testing used? standard used? measures?

Kothari 10 2008 ! ! # ! ! !

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

Kim 11 2008 ! ! ! ! ! #
Ho 12 2010 ! ! ! ! ! !
Lee SJ 13 2011 ! ! ! ! ! #
Lu PL 14 2012 ! # # ! ! !
Lee DS 15 2013 ! ! ! ! ! #
Chen 16 2013 ! ! ! ! ! #
Mitchell 17 2014 ! # # ! ! !
Niranjan 18 2014 ! ! # ! ! #
Kapur 19 2014 ! ! ! ! ! #
Hossain 20 2014 ! # # ! ! #
Senadheera 21 2016 ! ! ! ! ! #
Fasugba 22 2016 ! ! ! ! ! !
Amornchai- 23 2016 ! ! ! # # #
charoensuk
Jean 24 2016 ! ! # ! ! !
Adeep 25 2016 ! ! ! ! ! !
Mishra 26 2016 ! ! # ! ! #
Pruetpongpun 27 2017 ! ! ! ! ! #
Fernando 28 2017 ! ! # ! ! #
Sugianli 29 2017 ! ! ! ! ! !
Veeraraghavan 30 2018 ! # # ! ! !
Choe HS 31 2018 ! # ! # ! #
Lee H 32 2018 ! ! # ! ! #
Ganesh 33 2019 ! ! ! ! ! !

Abbreviations: (!), yes; (#), no.

2. Report on patients in the Asia-Pacific region as defined by the United
Nations (Australia, Bangladesh, Bhutan, Brunei, Cambodia, China,
Hong Kong, Taiwan, Macau, Cook Islands, Democratic People’s
Republic of Korea, Fiji, India, Indonesia, Japan, Kiribati, Laos, Malaysia,
Maldives, Marshall Islands, Micronesia, Mongolia, Myanmar, Nauru,
Nepal, New Zealand, Niue, Palau, Papua New Guinea, Philippines,
Republic of Korea, Samoa, Singapore, Solomon Islands, Sri Lanka,
Thailand, Timor-Leste, Tonga, Tuvalu, Vanuatu and Vietnam).
3. Describe the surveillance approach (population- and/or laboratory-
based).
4. Describe the microbiology procedures for identification and susceptibil-
ity testing.
5. Report the percentage of resistance to an antimicrobial drug with
information on total number of isolates tested.
6. Published in English language.
Studies were excluded if they (1) reported on outbreaks, (2) reported on
isolates obtained from animals, environment or food, (3) reported a sys-
tematic review, case series or a case report, or (4) lacked information
regarding clinical suspicion of UTI at isolate level.
Selection procedure
Two authors (A.K.S., F.G.) screened the title and abstract of all the articles
identified through the search strategy independently. Any discrepancies
during the screening process were resolved through consensus between
the two assessors. Full-text of articles was assessed by a single author
(A.K.S.), but two additional authors (C.S., F.vL.) were consulted to reach
consensus when uncertainty on inclusion arose.
Data extraction
Data extraction was done using a predesigned data collection tool, devel-
oped for the purpose of this review, and information stored in Microsoft
Excel 2017. Data extracted included article information (first author, year of
publication, time period of data collection, and country where surveillance
was carried out), study design (population-based and/or laboratory-based,
retrospective or prospective, sample size, age group, number of specimens
collected), pathogen identification method (E. coli and K. pneumoniae) and
antimicrobial susceptibility test (AST) methodology (instrument, guideline
used for breakpoints, and quality control), and antimicrobial resistance
data. Resistance data included total number of isolates obtained, number

3 of 12
Systematic review

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

Figure 2. Point prevalence estimates of resistance to nitrofurantoin in E. coli and K. pneumoniae by country in the Asia-Pacific region, stratified by sur-
veillance strategy (laboratory-based surveillance, population-based surveillance). The horizontal line indicates the 95% CI. An asterisk (*) indicates
the study only included ESBL-producing isolates.

Figure 3. Point prevalence estimates of resistance to fosfomycin in E. coli by country in the Asia-Pacific region, stratified by surveillance strategy (la-
boratory-based surveillance, population-based surveillance). The horizontal line indicates the 95% CI.

4 of 12
Systematic review
Figure 4. Point prevalence estimates of resistance to co-trimoxazole in E. coli and K. pneumoniae by country in the Asia-Pacific region, stratified by
surveillance strategy (laboratory-based surveillance, population-based surveillance). The horizontal line indicates the 95% CI.
of isolates tested, and the number of resistant strains per bacterial species
(E. coli and K. pneumoniae). We followed WHO GLASS for listing of anti-
microbial drugs.8 The antimicrobial susceptibility test results were collected
for co-trimoxazole (SXT), ciprofloxacin (CIP), levofloxacin (LVX), ceftriaxone
(CRO), cefotaxime (CTX), ceftazidime (CAZ), cefepime (FEP), imipenem
(IPM), meropenem (MEM), ertapenem (ETP), doripenem (DOR), colistin (CT),
fosfomycin (FOS), and nitrofurantoin (NIT), as susceptible, intermediate or
resistant, as reported in the original article. For studies reporting resistance
prevalence data for multiple populations, e.g. outpatients and inpatients,
data were extracted for each study population; this implied having a larger
number of prevalence data than the number of studies included.
Quality assessment
The quality of each article was assessed using a Newcastle-Ottawa Quality
Assessment Scale, modified for the purposes of this study (Supplementary
data, Methods 2).9 We assessed the following quality criteria: (1) definition
of study population; (2) representativeness of the sample; and (3) ascer-
tainment of AST method.
Data analysis
All extracted data were used directly, or recalculated as a prevalence of re-
sistance for each antimicrobial drug assessed. Intermediate susceptibility
test results were classified as resistant. The prevalence of resistance is
JAR
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
reported as a point estimate with its associated 95% CI. Given the aim of
the study to inform empirical treatment decisions, a combined analysis for
E. coli and K. pneumoniae was done for each study. However, the number of
E. coli and K. pneumoniae isolates contributing to each study was reported
to assess the relative contribution of each species to the overall data. Data
are reported stratified by surveillance strategy, i.e. laboratory-based surveil-
lance (LBS) and population-based surveillance (PBS). We defined a study as
population-based if the reported data were obtained from a defined popu-
lation with signs and symptoms indicating suspicion of UTI. A study was
defined as laboratory-based if data were obtained as part of routine diag-
nostic laboratory procedures of urine samples submitted to the laboratory
because of a clinical suspicion of UTI.
Studies that provided aggregated data from multiple countries are
reported separately. We did not conduct a meta-analysis because of the
small number of studies available per country, and the anticipated large
variation in study protocols between countries. Statistical analyses and
visualization of reported data and graph were performed using STATA v12
(STATA, TX, USA).
Results
In total, 2400 articles were identified of which 24 studies10–33 met
the inclusion criteria and were included in the final analysis
(Figure 1). Data are reported for 12 population-based surveillance
5 of 12
Systematic review

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

Figure 5. Point prevalence estimates of resistance to fluoroquinolones in E. coli and K. pneumoniae by country in the Asia-Pacific region, stratified by
surveillance strategy (laboratory-based surveillance, population-based surveillance): (a) ciprofloxacin; (b) levofloxacin. The horizontal line indicates
the 95% CI. An asterisk (*) indicates the study only included ESBL-producing isolates.

studies and 12 laboratory-based surveillance studies which Prevalence of AMR

originated from 11 countries. Studies were carried out between
2008 and 2019 and included between 47 and 7491 isolates
that were studied prospectively (21 studies) or retrospectively
(3 studies). Nine studies only reported data for E. coli and not for
K. pneumoniae (Table S1). Studies described AMR data in a range
of patient populations, including in- and out-patients, patients
with and without urinary catheters, and patients with lower and
upper UTIs (Table S1). Three articles reported on aggregated data
for multiple countries (Table S4).
Quality assessment
Nineteen out of 24 (79%) articles described the inclusion criteria of
the study conducted. Fourteen of 24 (58%) articles described the
sampling procedure, whilst 13 (54%) reported the microorganism
identification procedure. Almost all articles (22/24; 92%) described
the laboratory guidelines for the procedure of AST and the
breakpoints used, but the quality control procedure was only
reported in 10 (42%) of the articles (Table 1). Studies reported per-
centage of isolates susceptible or resistant, and only five studies
reported on intermediate test results (Tables S2 and S3).
The most frequently reported susceptibility data were for co-
trimoxazole, ciprofloxacin, ceftriaxone and nitrofurantoin, as the
most commonly used antimicrobial drugs to treat UTI. No studies
reported data for doripenem or colistin. Nitrofurantoin and fosfo-
mycin are considered the preferred oral antimicrobial drugs in sev-
eral guidelines for UTI treatment.34,35 The prevalence of resistance
to nitrofurantoin from PBS12,21,28,29,33 and LBS,10,17,18,22,25,26
ranged between 7.7% and 31.4%, and 2.7% and 29.5%, respect-
ively, except for a study from Sri Lanka in 2017 which showed a
high prevalence of resistance to nitrofurantoin (54.1%) (Figure 2).
The prevalence of resistance to fosfomycin in E. coli was reported
in only two studies, one each from Indonesia (1.63%) and Hong
Kong (1.8%) (Figure 3).12,29
The prevalence of resistance to co-trimoxazole ranged be-
tween 20.4% and 73.9% in LBS10,17,18,20,22,25,26,32 and between
29.4% and 67.7% in PBS.11–13,15,16,21,23,27,29,33 A high prevalence of
resistance to co-trimoxazole from LBS was observed in studies
from Bangladesh (58.0%), Bhutan (52.9%), and India (between
64.2% and 73.9%). High prevalence of resistance to co-
trimoxazole from PBS was reported in studies from Indonesia
(67.7%) and Thailand (between 60.2% and 61.7%) (Figure 4).

6 of 12
Systematic review
Figure 5. Continued.
The prevalence of resistance to ciprofloxacin from LBS10,17–
20,22,30,32
and PBS11–13,15,21,23,28,29 ranged between 6.3% and
79.6%, and 12.9% and 90.1%, respectively, with high prevalence
in Bangladesh, India, Sri Lanka, and Indonesia (Figure 5a). Five
studies reported resistance to levofloxacin in both LBS and PBS
which ranged between 34.8% and 71.3%, and 15.2% and 71.5%,
respectively (Figure 5b).13,16,26,29,30
The prevalence of resistance to ceftriaxone and cefotaxime
from LBS17,20,25,26,30,32 and PBS,13,15,16,23,27,29,33 ranged between
4.3% and 74.7%, and 7.1% and 72.3%, respectively (Figure 6a and
b). High resistance prevalence estimates of ceftriaxone and cefo-
taxime were observed in studies from Bangladesh (61.7%),
India (75.1%) and in Indonesia (72.3%). A similar wide range
of point prevalence estimates was observed for the other com-
monly used third-generation cephalosporin, ceftazidime
(Figure 6c).15,17,20,23,26,29,30,32
Studies that reported on the prevalence of resistance to carba-
penems were limited, in both PBS15,16,28,29 and LBS18,20,30,32
(Figure 7). Prevalence of resistance to imipenem, ertapenem and
meropenem from PBS reached up to 25% in a study from Sri
Lanka. A high prevalence of resistance to meropenem (51.7%)
from LBS was observed in a study from Bangladesh (Figure 7c).
Discussion
We performed a systematic review of studies reporting on the
prevalence of AMR in urinary pathogens in the Asia-Pacific region,
with a focus on E. coli and K. pneumoniae, according to WHO rec-
ommendations.2 We observed high AMR prevalence estimates
JAR
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
across the different classes of antimicrobial drugs that are used for
the treatment of UTIs, except for fosfomycin. Ciprofloxacin and co-
trimoxazole were the antimicrobial drugs most commonly
reported, reflecting their frequent use as first line and empirical
treatment in most hospital and/or community settings for treating
UTIs.4,5,34 However, our systematic search, which targeted 41
countries over a 12 year period, only yielded 24 studies that
fulfilled the inclusion criteria. We have previously noted a similar
paucity of surveillance studies on AMR in UTIs in a systematic re-
view on AMR in clinical syndromes in the African region.36 As noted
then, the paucity of data is surprising given that urine culture is
relatively easy to perform, both with respect to obtaining a
sample and to laboratory requirements, and AMR in urinary
pathogens from out-patients can give an indication of resist-
ance prevalence in the community in general. We included
studies from 11 countries in the APAC region, with a limited
number of countries contributing the majority of studies, includ-
ing India, Bangladesh, Sri Lanka, Thailand, Indonesia, Australia
and Republic of Korea. These data suggest that in the majority
of APAC countries, patients receive empirical treatment of
UTIs in the absence of published national surveillance data to
inform treatment strategies.
We reported the results for E. coli and K. pneumoniae combined
as this is most informative for empirical treatment, given
the predominant contribution of these two pathogens to UTI.
We included studies that performed LBS and PBS and which
included a range of patient populations, including in- and outpa-
tients, patients with urinary catheters, and patients with lower and
upper, and complicated and uncomplicated UTIs (Table S1) with
7 of 12
Systematic review

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

Figure 6. Point prevalence estimates of resistance against cephalosporins in E. coli and K. pneumoniae by country in the Asia-Pacific region, stratified
by surveillance strategy (laboratory-based surveillance, population-based surveillance): (a) ceftriaxone; (b) cefotaxime; (c) ceftazidime. The horizontal
line indicates the 95% CI.

8 of 12
Systematic review
Figure 6. Continued.
risk of bias, as previously reported.37–40 However, whilst the data
represent two bacterial species isolated from urinary samples
only, the high prevalence estimates reported from India,
Bangladesh and Sri Lanka are consistent with the high prevalence
of resistance reported from a range of surveillance studies and
programmes addressing other clinical syndromes and pathogens
from these countries.4,41,42
We assessed the quality of articles and found only a limited
number of studies that reported on the presence of quality control
procedures for AST. Although most of the laboratories reported the
guidelines used for susceptibility testing and breakpoints, variation
in quality of identification and susceptibility testing may contribute
to variation in prevalence estimates.43 In addition, inconsistent
reporting of susceptibility test results precluded an analysis by sus-
ceptible, intermediate and resistant test result categories, which
may have inflated resistance prevalence estimates because, if
intermediate test results were available, intermediate susceptible
test results were classified as resistant. These results further reflect
the need for standardized and quality laboratory procedures
and reporting.44
Our review has several limitations. First, we were unable to
retrieve some articles, despite our access to major online database
and medical libraries. In addition, we reported data from
community-based and hospital-associated as well as in- and out-
patients combined, for both laboratory-based and population-
based surveillance of UTIs. Second, we found heterogeneity across
the studies which precluded a meaningful analysis of trends over
time, even within countries. For example, five studies from India
JAR
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
each reported data from different populations, i.e. from adult
female patients in the out-patient department (OPD); from in-
patients; from male and female patients attending OPD; from
paediatric in- and out-patients, and for Gram-negative isolates
from unspecified populations (Table S1). Furthermore, there is vari-
ation in the antibiotics included in the studies. Therefore, it would
not be possible to interpret the results of a combined analysis of
trends over time. For the same reason, a direct comparison be-
tween LBS and PBS data is not possible, although Figures 2 and 4–7
suggest that LBS prevalence estimates are higher than PBS.
However, in a direct comparison in a study in Indonesia40 it was
demonstrated that LBS estimates indeed tend to be biased
towards higher prevalence of resistance compared with PBS.
In conclusion, the results of our systematic review show high
prevalence among uropathogens of AMR to co-trimoxazole and
ciprofloxacin, which are commonly used for the empirical treat-
ment of UTI, in most of the countries in the APAC for which data
are available. The main treatment option appears to be fosfomycin
as recommended in several guidelines, which is not always access-
ible for patients.34,35 The high prevalence estimates of AMR are
observed in countries which have only recently developed or
implemented their national surveillance system, such as
Indonesia, and Bangladesh and India, respectively. For most other
countries in the region, AMR surveillance data on urinary patho-
gens are still lacking. Clearly, whilst AMR surveillance is crucial to
understand the burden of AMR and to inform empirical treatment,
novel feasible and affordable approaches that facilitate
population-based AMR surveillance, such as previously reported,7
9 of 12
Systematic review

Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021

Figure 7. Point prevalence estimates of resistance against carbapenems in E. coli and K. pneumoniae by country in the Asia-Pacific region, stratified
by surveillance strategy (laboratory-based surveillance, population-based surveillance): (a) imipenem, (b) ertapenem, (c) meropenem. The horizontal
line indicates the 95% CI. An asterisk (*) indicates the study only included ESBL isolates.

10 of 12
Systematic review
Figure 7. Continued.
are needed to provide reproducible local AMR prevalence esti-
mates to inform empirical treatment guidelines and to contribute
to national surveillance data to monitor trends.
Funding
This work was supported by grant of the Royal Netherlands Academy of
Arts and Sciences as part of the Scientific Program Indonesia-the
Netherlands (SPIN) (project number: SPIN3-JRP-30).
Transparency declarations
None to declare.
Author contributions
A.K.S. and C.S. conceived the study. A.K.S., C.S. and F.vL. designed the study.
A.K.S. and F.G. searched published work, reviewed published papers and
made the primary selection of eligible papers. C.S. and F.vL. resolved dis-
agreements regarding the eligibility of papers. A.K.S. and C.S. compiled the
data. A.K.S., C.S. and F.vL. analysed the data. All authors contributed to the
writing of the report and have seen and approved the final version.
Supplementary data
Supplementary Methods and Tables S1 to S4 are available as
Supplementary data at JAC-AMR Online.
References
1 World Health Organization. Global antimicrobial resistance surveillance
system (GLASS) report: early implementation. 2020. https://apps.who.int/iris/
bitstream/handle/10665/332081/9789240005587-eng.pdf?ua"1.
JAR
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
2 World Health Organization. Global Action Plan on Antimicrobial
Resistance. 2015. http://www.who.int/iris/bitstream/10665/193736/1/
9789241509763_eng.pdf?ua"1.
3 Zellweger RM, Carrique-Mas J, Limmathurotsakul D et al. A current per-
spective on antimicrobial resistance in Southeast Asia. J Antimicrob
Chemother 2017; 72: 2963–72.
4 Yam ELY, Hsu LY, Yap EP-H et al. Antimicrobial Resistance in the Asia Pacific
region: a meeting report. Antimicrob Resist Infect Control 2019; 8: 1–12.
5 Paul R. State of the globe: Rising antimicrobial resistance of pathogens in
urinary tract infection. J Global Infect Dis 2018; 10: 117–8.
6 Ahmed SS, Shariq A, Alsalloom AA et al. Uropathogens and their antimicro-
bial resistance patterns: Relationship with urinary tract infections. Int J Health
Sci 2019; 13: 48–55.
7 Ginting F, Sugianli AK, Bijl G et al. Rethinking antimicrobial resistance sur-
veillance: a role for lot quality assurance sampling. Am J Epidemiol 2019; 188:
734–42.
8 World Health Organization. Global Antimicrobial Resistance Surveillance
System: Manual for Early Implementation. 2015. https://apps.who.int/iris/bit
stream/handle/10665/188783/9789241549400_eng.pdf?sequence"1.
9 Herzog R, Álvarez-Pasquin MJ, Dı́az C et al. Are healthcare workers’ inten-
tions to vaccinate related to their knowledge, beliefs and attitudes? a system-
atic review. BMC Public Health 2013; 13: 17.
10 Kothari A, Sagar V. Antibiotic resistance in pathogens causing
community-acquired urinary tract infections in India: a multicenter study. J
Infect Dev Ctries 2008; 2: 354–8.
11 Kim ME, Ha U-S, Cho Y-H. Prevalence of antimicrobial resistance among
uropathogens causing acute uncomplicated cystitis in female outpatients in
South Korea: a multicentre study in 2006. Int J Antimicrob Agents 2008; 31:
15–8.
12 Ho P, Yip K-S, Chow K-H et al. Antimicrobial resistance among uropatho-
gens that cause acute uncomplicated cystitis in women in Hong Kong: a
11 of 12
Systematic review
prospective multicenter study in 2006 to 2008. Diagn Microbiol Infect Dis
2010; 66: 87–93.
13 Shim BS, Kim CS, Kim ME et al. Antimicrobial resistance in community-
acquired urinary tract infections: results from the Korean Antimicrobial
Resistance Monitoring System. J Infect Chemother 2011; 17: 440–6.
14 Lu P-L, Liu Y-C, Toh H-S et al. Epidemiology and antimicrobial susceptibil-
ity profiles of Gram-negative bacteria causing urinary tract infections in the
Asia-Pacific region: 2009–2010 results from the Study for Monitoring
Antimicrobial Resistance Trends (SMART. ). Int J Antimicrob Agents 2012; 40:
S37–43.
15 Lee DS, Choe H-S, Lee SJ et al. Antimicrobial susceptibility pattern and epi-
demiology of female urinary tract infections in South Korea, 2010-2011.
Antimicrob Agents Chemother 2013; 57: 5384–93.
16 Chen LF, Chiu C-T, Lo J-Y et al. Clinical characteristics and antimicrobial
susceptibility pattern of hospitalised patients with community-acquired urin-
ary tract infections at a regional hospital in Taiwan. Healthc Infect 2014; 19:
20–5.
17 Mitchell DH, Coombs GW, Daley DA. Community-onset Gram-negative
Surveillance Program annual report, 2012. Commun Dis Intell Q Rep 2014; 38:
E54–58.
18 Niranjan V, Malini A. Antimicrobial resistance pattern in Escherichia coli
causing urinary tract infection among inpatients. Indian J Med Res 2014; 139:
945–8.
19 Kapur S. Comparative Prevalence of antimicrobial resistance in
community-acquired urinary tract infection cases from representative states
of Northern and Southern India. J Clin Diagn Res 2014; 8: DC09–12.
20 Hossain MD, Ahsan S, Kabir MS. Antibiotic resistance patterns of uropath-
ogens isolated from catheterized and noncatheterized patients in Dhaka,
Bangladesh. Tzu Chi Med J 2014; 26: 127–31.
21 Senadheera GPSG, Sri Ranganathan S, Patabendige G et al. Resistance
and utilisation pattern of antibacterial agents in outpatient settings in two
Teaching Hospitals in Colombo. Ceylon Med J 2016; 61: 113–7.
22 Fasugba O, Mitchell BG, Mnatzaganian G et al. Five-year antimicrobial re-
sistance patterns of urinary Escherichia coli at an Australian Tertiary Hospital:
time series analyses of prevalence data. PLoS One 2016; 11: e0164306.
23 Amornchaicharoensuk Y. Clinical characteristics and antibiotic resistance
pattern of pathogens in pediatric urinary tract infection. Southeast Asian J
Trop Med Public Health 2016; 47: 976–82.
24 Jean S-S, Coombs G, Ling T et al. Epidemiology and antimicrobial suscep-
tibility profiles of pathogens causing urinary tract infections in the Asia-Pacific
region: Results from the Study for Monitoring Antimicrobial Resistance Trends
(SMART), 2010–2013. Int J Antimicrob Agents 2016; 47: 328–34.
25 Adeep M, Nima T, Kezang W et al. A retrospective analysis of the etiologic
agents and antibiotic susceptibility pattern of uropathogens isolated in the
Jigme Dorji Wangchuck National Referral Hospital, Thimphu, Bhutan. BMC Res
Notes 2016; 9: 6.
26 Mishra MP, Sarangi R, Padhy RN. Prevalence of multidrug resistant uropa-
thogenic bacteria in pediatric patients of a tertiary care hospital in eastern
India. J Infect Public Health 2016; 9: 308–14.
27 Pruetpongpun N, Khawcharoenporn T, Damronglerd P et al.
Inappropriate empirical treatment of uncomplicated cystitis in Thai women:
lessons learned. Clin Infect Dis 2017; 64: S115–8.
28 Fernando M, Luke WANV, Miththinda JKND et al. Extended spectrum beta
lactamase producing organisms causing urinary tract infections in Sri Lanka
12 of 12
and their antibiotic susceptibility pattern –a hospital based cross sectional
study. BMC Infect Dis 2017; 17: 1–6.
29 Sugianli AK, Ginting F, Kusumawati RL et al. Antimicrobial resistance in
uropathogens and appropriateness of empirical treatment: a population-
based surveillance study in Indonesia. J Antimicrob Chemother 2017; 72:
1469–77.
30 Veeraraghavan B, Jesudason MR, Prakash JAJ. Antimicrobial susceptibility
profiles of gram-negative bacteria causing infections collected across
India during 2014–2016: Study for monitoring antimicrobial resistance trend
report. Indian J Med Microbiol 2018; 36: 32–6.
31 Choe H-S, Lee S-J, Cho Y-H et al. Aspects of urinary tract infections and
Downloaded from https://academic.oup.com/jacamr/article/3/1/dlab003/6153836 by guest on 24 August 2021
antimicrobial resistance in hospitalized urology patients in Asia: 10-year
results of the Global Prevalence Study of Infections in Urology (GPIU). J Infect
Chemother 2018; 24: 278–83.
32 Lee H, Yoon E-J, Kim D et al. Antimicrobial resistance of major clinical
pathogens in South Korea, May 2016 to April 2017. First one-year report from
Kor-GLASS. Eurosurveillance 2018; 23: pii"1800047.
33 Ganesh R, Shrestha D, Bhattachan B et al. Epidemiology of urinary tract
infection and antimicrobial resistance in a pediatric hospital in Nepal. BMC
Infect Dis 2019; 19: 5.
34 European Association Urology. European Association of Urology
Guidelines. 2018 Edition. http://uroweb.org/guidelines/compilations-of-all-
guidelines/.
35 Gupta K, Hooton TM, Naber KG et al. International clinical practice guide-
lines for the treatment of acute uncomplicated cystitis and pyelonephritis in
women: a 2010 Update by the Infectious Diseases Society of America and
the European Society for Microbiology and Infectious Diseases. Clin Infect Dis
2011; 52: e103–20.
36 Leopold SJ, van Leth F, Tarekegn H et al. Antimicrobial drug resistance
among clinically relevant bacterial isolates in sub-Saharan Africa: a systemat-
ic review. J Antimicrob Chemother 2014; 69: 2337–53.
37 Laupland KB, Ross T, Pitout JDD et al. Investigation of sources of potential
bias in laboratory surveillance for anti-microbial resistance. Clin Invest Med
2007; 30: E159–66.
38 Rempel O, Pitout JDD, Laupland KB. Antimicrobial resistance surveillance
systems: are potential biases taken into account? Can J Infect Dis Med
Microbiol 2011; 22: e24–8.
39 Rempel OR, Laupland KB. Surveillance for antimicrobial resistant organ-
isms: potential sources and magnitude of bias. Epidemiol Infect 2009; 137:
1665–73.
40 Sugianli AK, Ginting F, Kusumawati RL et al. Laboratory-based versus
population-based surveillance of antimicrobial resistance to inform empirical
treatment for suspected urinary tract infection in Indonesia. PLoS One 2020;
15: e0230489.
41 Veeraraghavan B, Walia K. Antimicrobial susceptibility profile & resist-
ance mechanisms of Global Antimicrobial Resistance Surveillance System
(GLASS) priority pathogens from India. Indian J Med Res 2019; 149: 87–96.
42 Dharmapalan D, Shet A, Yewale V et al. High reported rates of antimicro-
bial resistance in Indian neonatal and pediatric blood stream infections.
J Pediatr Infect Dis Soc 2017; 6: e62–8.
43 Shah AS, Karunaratne K, Shakya G et al. Strengthening laboratory surveil-
lance of antimicrobial resistance in South East Asia. Bmj 2017; 358: j3474.
44 Vong S, Anciaux A, Hulth A et al. Using information technology to improve
surveillance of antimicrobial resistance in South East Asia. Bmj 2017; 358:
j3781.